Orchestrating A/P and D/V guidance - A Wnt/Netrin tale

References

• Ishii N, Wadsworth WG, Stern BD, Culotti JG, Hedgecock EM. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron (1992); 9:873-81; PMID:1329863; http://dx.doi.org/10.1016/0896-6273(92)90240-E
   PubMed Web of Science ®Google Scholar
• Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell (1999); 96:795-806; PMID:10102268; http://dx.doi.org/10.1016/S0092-8674(00)80590-5
   PubMed Web of Science ®Google Scholar
• Kidd T, Bland KS, Goodman CS. Slit is the midline repellent for the robo receptor in Drosophila. Cell (1999) 96:785-94; PMID:10102267; http://dx.doi.org/10.1016/S0092-8674(00)80589-9
   PubMed Web of Science ®Google Scholar
• Kennedy TE, Serafini T, de la Torre JR, Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell (1994) 78:425-35; PMID:8062385; http://dx.doi.org/10.1016/0092-8674(94)90421-9
   PubMed Web of Science ®Google Scholar
• Hao JC, Yu TW, Fujisawa K, Culotti JG, Gengyo-Ando K, Mitani S, Moulder G, Barstead R, Tessier-Lavigne M, Bargmann CI. C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron (2001) 32:25-38; PMID:11604136; http://dx.doi.org/10.1016/S0896-6273(01)00448-2
   PubMed Web of Science ®Google Scholar
• Silhankova M, Korswagen HC. Migration of neuronal cells along the anterior-posterior body axis of C. elegans: Wnts are in control. Curr Opin Genet Dev (2007); 17:320-5; PMID:17644372; http://dx.doi.org/10.1016/j.gde.2007.05.007
   PubMed Web of Science ®Google Scholar
• Inoue T, Oz HS, Wiland D, Gharib S, Deshpande R, Hill RJ, Katz WS, Sternberg PW. C. elegans LIN-18 is a Ryk ortholog and functions in parallel to LIN-17/Frizzled in Wnt signaling. Cell (2004) 118:795-806; PMID:15369677; http://dx.doi.org/10.1016/j.cell.2004.09.001
   PubMed Web of Science ®Google Scholar
• Zinovyeva AY, Yamamoto Y, Sawa H, Forrester WC. Complex network of Wnt signaling regulates neuronal migrations during Caenorhabditis elegans development. Genetics (2008); 179:1357-71; PMID:18622031; http://dx.doi.org/10.1534/genetics.108.090290
   PubMed Web of Science ®Google Scholar
• Hilliard MA, Bargmann CI. Wnt signals and frizzled activity orient anterior-posterior axon outgrowth in C. elegans. Dev Cell (2006); 10:379-90; PMID:16516840; http://dx.doi.org/10.1016/j.devcel.2006.01.013
   PubMed Web of Science ®Google Scholar
• Pan C.-L, Howell JE, Clark SG, Hilliard M, Cordes S, Bargmann CI, Garriga G. Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev Cell (2006); 10:367-77; PMID:16516839; http://dx.doi.org/10.1016/j.devcel.2006.02.010
   PubMed Web of Science ®Google Scholar
• Prasad BC, Clark SG. Wnt signaling establishes anteroposterior neuronal polarity and requires retromer in C. elegans. Development (2006); 133:1757-66; PMID:16571624; http://dx.doi.org/10.1242/dev.02357
   PubMed Web of Science ®Google Scholar
• Rhiner C, Gysi S, Fröhli E, Hengartner MO, Hajnal A. Syndecan regulates cell migration and axon guidance in C. elegans. Development (2005); 132:4621-33; PMID:16176946; http://dx.doi.org/10.1242/dev.02042
   PubMed Web of Science ®Google Scholar
• Merz DC, Alves G, Kawano T, Zheng H, Culotti JG. UNC-52/Perlecan affects gonadal leader cell migrations in c. elegans hermaphrodites through alterations in growth factor signaling. Dev Biol (2003); 256:174-187; http://dx.doi.org/10.1016/S0012-1606(03)00014-9
   Web of Science ®Google Scholar
• Schwabiuk M, Coudiere L, Merz DC. SDN-1/syndecan regulates growth factor signaling in distal tip cell migrations in C. elegans. Dev Biol (2009); 334:235-42; PMID:19631636; http://dx.doi.org/10.1016/j.ydbio.2009.07.020
   PubMed Web of Science ®Google Scholar
• Hedgecock EM, Culotti JG, Hall DH. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron (1990); 4:61-85; PMID:2310575; http://dx.doi.org/10.1016/0896-6273(90)90444-K
   PubMed Web of Science ®Google Scholar
• Wadsworth WG, Bhatt H, Hedgecock EM. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron (1996); 16:35-46; PMID:8562088; http://dx.doi.org/10.1016/S0896-6273(00)80021-5
   PubMed Web of Science ®Google Scholar
• Lai Wing Sun K, Correia JP, Kennedy TE. Netrins: versatile extracellular cues with diverse functions. Development (2011); 138:2153-69; PMID:21558366; http://dx.doi.org/10.1242/dev.044529
   PubMed Web of Science ®Google Scholar
• Honigberg L, Kenyon C. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development (2000); 127:4655-68; PMID:11023868
   PubMed Web of Science ®Google Scholar
• Middelkoop TC, Williams L, Yang PT, Luchtenberg J, Betist MC, Ji N, van Oudenaarden A, Kenyon C, Korswagen HC. The thrombospondin repeat containing protein MIG-21 controls a left-right asymmetric Wnt signaling response in migrating C. elegans neuroblasts. Dev Biol (2012); 361:338-48; PMID:22074987; http://dx.doi.org/10.1016/j.ydbio.2011.10.029
   PubMed Web of Science ®Google Scholar
• Teichmann HM, Shen K. UNC-6 and UNC-40 promote dendritic growth through PAR-4 in Caenorhabditis elegans neurons. Nat Neurosci (2011); 14:165-72; PMID:21186357; http://dx.doi.org/10.1038/nn.2717
   PubMed Web of Science ®Google Scholar
• Levy-Strumpf N, Culotti JG. VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions of UNC-40 in C. elegans. Nat Neurosci (2007); 10:161-8; PMID:17237777; http://dx.doi.org/10.1038/nn1835
   PubMed Web of Science ®Google Scholar
• Watari-Goshima N, Ogura K, Wolf FW, Goshima Y, Garriga GC. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations. Nat Neurosci (2007); 10:169-76; PMID:17237778; http://dx.doi.org/10.1038/nn1834
   PubMed Web of Science ®Google Scholar
• Levy-Strumpf N, Culotti JG. Netrins and Wnts Function Redundantly to Regulate Antero-Posterior and Dorso-Ventral Guidance in C. elegans. PLoS Genet (2014); 10:e1004381; PMID:24901837; http://dx.doi.org/10.1371/journal.pgen.1004381
   PubMed Web of Science ®Google Scholar
• Wong M-C, Schwarzbauer JE. Gonad morphogenesis and distal tip cell migration in the Caenorhabditis elegans hermaphrodite. Wiley Interdiscip. Rev Dev Biol (2012); 1:519-531
   Web of Science ®Google Scholar
• Harterink M, Kim DH, Middelkoop TC, Doan TD, van Oudenaarden A, Korswagen HC. Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein. Development (2011); 138:2915-24; PMID:21653614; http://dx.doi.org/10.1242/dev.064733
   PubMed Web of Science ®Google Scholar
• Su M, Merz DC, Killeen MT, Zhou Y, Zheng H, Kramer JM, Hedgecock EM, Culotti JG. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development (2000); 127:585-94; PMID:10631179
   PubMed Web of Science ®Google Scholar
• Nishiwaki K. Mutations affecting symmetrical migration of distal tip cells in Caenorhabditis elegans. Genetics (1999); 152:985-97; PMID:10388818
   PubMed Web of Science ®Google Scholar
• Cabello J, Neukomm LJ, Günesdogan U, Burkart K, Charette SJ, Lochnit G, Hengartner MO, Schnabel R. The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. PLoS Biol (2010); 8:e1000297; PMID:20126385; http://dx.doi.org/10.1371/journal.pbio.1000297
   PubMed Web of Science ®Google Scholar
• Yang P-T, Lorenowicz MJ, Silhankova M, Coudreuse DY, Betist MC, Korswagen HC. Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells. Dev Cell (2008); 14:140-7
   PubMed Web of Science ®Google Scholar
• Green JL, Inoue T, Sternberg PW. Opposing Wnt pathways orient cell polarity during organogenesis. Cell (2008); 134:646-56; PMID:18724937; http://dx.doi.org/10.1016/j.cell.2008.06.026
   PubMed Web of Science ®Google Scholar
• Levy-Strumpf N, Krizus M, Zheng H, Brown L, Culotti JG. The Wnt Frizzled Receptor MOM-5 Regulates the UNC-5 Netrin Receptor through Small GTPase-Dependent Signaling to Determine the Polarity of Migrating Cells. PLOS Genet (2015); 11:e1005446; PMID:26292279; http://dx.doi.org/10.1371/journal.pgen.1005446
   PubMed Web of Science ®Google Scholar
• Jaworski A, Tom I, Tong RK, Gildea HK, Koch AW, Gonzalez LC, Tessier-Lavigne M. Operational redundancy in axon guidance through the multifunctional receptor Robo3 and its ligand NELL2. Science (2015); 350:961-965; PMID:26586761; http://dx.doi.org/10.1126/science.aad2615
   PubMed Web of Science ®Google Scholar
• Kulkarni G, Xu Z, Mohamed AM, Li H, Tang X, Limerick G, Wadsworth WG. Experimental evidence for UNC-6 (netrin) axon guidance by stochastic fluctuations of intracellular UNC-40 (DCC) outgrowth activity. Biol Open 6 (2013); 2(12):1300-12
   PubMed Web of Science ®Google Scholar
• Hamelin M, Zhou Y, Su MW, Scott IM, Culotti JG. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steer their axons dorsally. Nature (1993); 364:327-30; PMID:8332188; http://dx.doi.org/10.1038/364327a0
   PubMed Web of Science ®Google Scholar
• Leung-Hagesteijn C, Spence AM, Stern BD, Zhou Y, Su MW, Hedgecock EM, Culotti JG. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell (1992); 71:289-99; PMID:1384987; http://dx.doi.org/10.1016/0092-8674(92)90357-I
   PubMed Web of Science ®Google Scholar
• Sawa H, Korswagen HC. Wnt signaling in C. elegans. WormBook 1–30 (2013).
   Google Scholar
• Mehlen P, Furne C. Netrin-1: when a neuronal guidance cue turns out to be a regulator of tumorigenesis. Cell Mol Life Sci (2005); 62:2599-616; PMID:16158190; http://dx.doi.org/10.1007/s00018-005-5191-3
   PubMed Web of Science ®Google Scholar
• Baker KA, Moore SW, Jarjour AA, Kennedy TE. When a diffusible axon guidance cue stops diffusing: roles for netrins in adhesion and morphogenesis. Curr Opin Neurobiol (2006); 16:529-34; PMID:16935486; http://dx.doi.org/10.1016/j.conb.2006.08.002
   PubMed Web of Science ®Google Scholar
• Cirulli V, Yebra M. Netrins: beyond the brain. Nat Rev Mol Cell Biol (2007); 8:296-306; PMID:17356579; http://dx.doi.org/10.1038/nrm2142
   PubMed Web of Science ®Google Scholar
• Poon VY, Klassen MP, Shen K. UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature (2008); 455:669-73; PMID:18776887; http://dx.doi.org/10.1038/nature07291
   PubMed Web of Science ®Google Scholar
• Ziel J, Sherwood D. Roles for netrin signaling outside of axon guidance: a view from the worm. Dev Dyn (2010); 239:1296-1305; PMID:20108323
   PubMed Web of Science ®Google Scholar
• Ziel JJW, Hagedorn EEJ, Audhya A, Sherwood DDR. UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat Cell Biol (2009); 11:183-9; PMID:19098902; http://dx.doi.org/10.1038/ncb1825
   PubMed Web of Science ®Google Scholar
• Colón-Ramos DA, Margeta MA, Shen K. Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science (2007); 318:103-6; PMID:Can't; http://dx.doi.org/10.1126/science.1143762
   PubMedGoogle Scholar
• Ciani L, Salinas PC. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci (2005); 6:351-62; PMID:15832199; http://dx.doi.org/10.1038/nrn1665
   PubMed Web of Science ®Google Scholar
• Fradkin LG, Garriga G, Salinas PC, Thomas JB, Yu X, Zou Y. Wnt signaling in neural circuit development. J Neurosci (2005); 25:10376-8; PMID:16280576; http://dx.doi.org/10.1523/JNEUROSCI.3429-05.2005
   PubMed Web of Science ®Google Scholar
• Park M, Shen K. WNTs in synapse formation and neuronal circuitry. EMBO J (2012); 31:2697-704; PMID:22617419; http://dx.doi.org/10.1038/emboj.2012.145
   PubMed Web of Science ®Google Scholar
• Herr P, Hausmann G, Basler K. WNT secretion and signalling in human disease. Trends Mol Med (2012); 18:483-93; PMID:22796206; http://dx.doi.org/10.1016/j.molmed.2012.06.008
   PubMed Web of Science ®Google Scholar
• Polakis P. Wnt signaling in cancer. Cold Spring Harb Perspect Biol (2012); 4(5):4:pii: a008052; PMID:22438566; http://dx.doi.org/10.1101/cshperspect.a008052.
   PubMed Web of Science ®Google Scholar
• Bhat RA, Stauffer B, Komm BS, Bodine PVN. Structure-function analysis of secreted frizzled-related protein-1 for its Wnt antagonist function. J Cell Biochem (2007); 102:1519-28; PMID:17471511; http://dx.doi.org/10.1002/jcb.21372
   PubMed Web of Science ®Google Scholar
• Coudreuse DYM, Roël G, Betist MC, Destrée O, Korswagen HC. Wnt gradient formation requires retromer function in Wnt-producing cells. Science (2006); 312:921-4; PMID:16645052; http://dx.doi.org/10.1126/science.1124856
   PubMed Web of Science ®Google Scholar